Mate limitation in sea lice infesting wild salmon hosts: the influence of parasite sex ratio and aggregation

Mate limitation in dioecious parasite species has the potential to impact parasite population growth. Our focus of interest was the influence of parasite sex distribution among hosts on parasite reproduction and transmission dynamics for populations of ectoparasitic sea lice (Lepeophtheirus salmonis Kroyer) establishing on wild juvenile salmon hosts. The data included more than 139,000 out-migrating juvenile pink salmon (Oncorhynchus gorbuscha (Walbaum)) and chum salmon (Oncorhynchus keta (Walbaum)) in British Columbia, Canada, sampled over nine years. For almost all years, the sex ratio of the reproductive stages of the sea lice was female-biased. The probability of a female being able to mate (i.e., of being attached to a fish also carrying a male louse) increased with increasing parasite abundance and parasite aggregation. We compared, with expected modeling predictions, the observed prevalence of pairs of sea lice (i.e., one reproductive louse of each sex) on a given fish and the observed probability of a female being able to mate. These comparisons showed that male and female sea lice tend to be distributed together rather than separately on hosts. Distribution together means that sea lice are distributed randomly on hosts according to a common negative binomial distribution, whereas distribution separately means that males are distributed according to a negative binomial and females are distributed in their own negative binomial among hosts. Despite the tendency for distribution together we found that, in every year, at least 30% of reproductive female sea lice experience mate limitation. This Allee effect will result in submaximal rates of parasite reproduction at low parasite abundances and may limit parasite transmission. The work has important implications for salmon parasite management and the health both of captive farm salmon populations and migratory wild stocks. More broadly, these results demonstrate the potential impact of mate limitation as a constraint to the establishment and spread of wild ectoparasite populations.